Skip to main content

Facilitation of Australia’s southernmost reef-building coral by sea urchin herbivory

Abstract

Competition for space between corals and macroalgae represents a key threatening process for coral reefs, yet the influence of climate change on this competitive interaction is poorly understood, particularly at the poleward margins of coral distribution. Here we describe the discovery of Australia’s southernmost hermatypic corals and explore novel dynamics facilitating the presence and extent of high-latitude coral communities. Examination of 607 shallow reef sites across temperate Australia revealed hard corals to be negatively associated with increasing kelp bed cover, but positively associated with increasing sea surface temperature, herbivorous fishes, grazing sea urchins, and increasing cover of turf algae, which proliferates in the absence of kelp. However, the nature of these effects varied across different regions of temperate Australia consistent with regional variability in the presence/absence of key functional groups for temperate reefs, such as guilds of subtropical herbivorous fishes and/or prevalence of overgrazing sea urchins. For the southernmost coral communities, in eastern Bass Strait Tasmania, the dominant reef-building coral Plesiastrea versipora was negatively associated with kelp and positively associated with the southward range-extending diadematid sea urchin Centrostephanus rodgersii, which has caused extensive kelp bed overgrazing since first locally reported in 1974. Facilitation of coral establishment was strongest on overgrazed barrens where urchin density was relatively low, but sufficient to maintain the reef kelp-free, while corals were less frequent at high urchin densities and completely absent from barrens colonised by intensively grazing limpets. In contrast to tropical Australian coral reefs and other temperate regions (e.g. Western Australia), assays of herbivory confirmed sea urchin grazing, not herbivorous fishes, as chiefly responsible for kelp consumption within this high-latitude system. Size structure of P. versipora in eastern Bass Strait was dominated by small colonies (~ 20 cm2), suggesting an expanding population at the poleward edge of the species’ range. Nevertheless, colonies up to a maximum area of 500 cm2 were observed, which are likely > 40 yrs old based on growth rates established in warmer waters. This research highlights novel patterns and processes structuring the interface between subtropical and temperate reef communities under climate change and specifically highlights the role of herbivores in releasing corals from competition with kelp under warming ocean regimes.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Andrew NL, Jones GP (1990) Patch formation by herbivorous fish in a temperate Australian kelp forest. Oecologia 85:57–68

    Article  CAS  PubMed  Google Scholar 

  2. Babcock R, Shears N, Alcala A, Barrett N, Edgar G, Lafferty K, McClanahan T, Russ G (2010) Decadal trends in marine reserves reveal differential rates of change in direct and indirect effects. Proceedings of the National Academy of Sciences 107:18256–18261

    Article  Google Scholar 

  3. Bates AE, Barrett NS, Stuart-Smith RD, Holbrook NJ, Thompson PA, Edgar GJ (2014) Resilience and signatures of tropicalization in protected reef fish communities. Nature Climate Change 4:62

    Article  Google Scholar 

  4. Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827

    Article  CAS  PubMed  Google Scholar 

  5. Bellwood DR, Hoey AS, Ackerman JL, Depczynski M (2006) Coral bleaching, reef fish community phase shifts and the resilience of coral reefs. Global Change Biology 12:1587–1594

    Article  Google Scholar 

  6. Bennett S, Wernberg T, Harvey ES, Santana-Garcon J, Saunders BJ (2015) Tropical herbivores provide resilience to a climate-mediated phase shift on temperate reefs. Ecology Letters 18:714–723

    Article  PubMed  Google Scholar 

  7. Birrell CL, McCook LJ, Willis BL (2005) Effects of algal turfs and sediment on coral settlement. Marine Pollution Bulletin 51:408–414

    Article  CAS  PubMed  Google Scholar 

  8. Burgess S, McCulloch M, Mortimer G, Ward T (2009) Structure and growth rates of the high-latitude coral: Plesiastrea versipora. Coral Reefs 28:1005

    Article  Google Scholar 

  9. Carpenter RC, Edmunds PJ (2006) Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals. Ecology letters 9:271–280

    Article  PubMed  Google Scholar 

  10. Cresswell AK, Edgar GJ, Stuart-Smith RD, Thomson RJ, Barrett NS, Johnson CR (2017) Translating local benthic community structure to national biogenic reef habitat types. Global Ecology and Biogeography 26:1112–1125

    Article  Google Scholar 

  11. Downie RA, Babcock RC, Thomson DP, Vanderklift MA (2013) Density of herbivorous fish and intensity of herbivory are influenced by proximity to coral reefs. Marine Ecology Progress Series 482:217–225

    Article  Google Scholar 

  12. Edgar GJ, Barrett NS (1999) Effects of the declaration of marine reserves on Tasmanian reef fishes, invertebrates and plants. Journal of Experimental Marine Biology and Ecology [J Exp Mar Biol Ecol] 242:107–144

    Article  Google Scholar 

  13. Edmunds PC, Carpenter RC (2001) Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef. Proceedings of the National Academy of Sciences 98:5067–5071

    Article  CAS  Google Scholar 

  14. Grömping U (2006) Relative importance for linear regression in R: the package relaimpo. Journal of Statistical Software 17:1–27

    Article  Google Scholar 

  15. Hoey AS, Bellwood DR (2009) Limited functional redundancy in a high diversity system: single species dominates key ecological process on coral reefs. Ecosystems 12:1316–1328

    Article  Google Scholar 

  16. Hoey AS, Bellwood DR (2011) Suppression of herbivory by macroalgal density: a critical feedback on coral reefs? Ecology letters 14:267–273

    Article  PubMed  Google Scholar 

  17. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R et al (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377

    Article  CAS  PubMed  Google Scholar 

  18. Irving AD, Connell SD (2006) Physical disturbance by kelp abrades erect algae from the understorey. Marine Ecology Progress Series 324:127–137

    Article  Google Scholar 

  19. Johnson CR, Ling S, Ross D, Shepherd S, Miller K (2005) Establishment of the long-spined sea urchin (Centrostephanus rodgersii) in Tasmania: first assessment of potential threats to fisheries. Fisheries Research and Development Corporation Final Report, Project No. 2001/044, University of Tasmania, Hobart, Tasmania, Australia

  20. Johnson CR, Banks SC, Barrett NS, Cazassus F, Dunstan PK, Edgar GJ, Frusher SD, Gardner C, Haddon M, Helidoniotis F (2011) Climate change cascades: shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania. Journal of Experimental Marine Biology and Ecology 400:17–32

    Article  Google Scholar 

  21. Jones GP (1992) Interactions between herbivorous fishes and macroalgae on a temperate rocky reef. Journal of Experimental Marine Biology and Ecology 159:217–235

    Article  Google Scholar 

  22. Jones GP, Andrew NL (1990) Herbivory and patch dynamics on rocky reefs in temperate Australasia: the roles of fish and sea urchins. Australian Journal of Ecology 15:505–520

    Article  Google Scholar 

  23. Kriegisch N, Reeves S, Johnson CR, Ling SD (2016) Phase-shift dynamics of sea urchin overgrazing on nutrified reefs. PloS one 11:e0168333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ling S (2008) Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state. Oecologia 156:883–894

    Article  CAS  PubMed  Google Scholar 

  25. Ling S, Ibbott S, Sanderson J (2010) Recovery of canopy-forming macroalgae following removal of the enigmatic grazing sea urchin Heliocidaris erythrogramma. J Exp Mar Biol Ecol 395:135–146

    Article  Google Scholar 

  26. Ling S, Johnson C, Frusher S, King C (2008) Reproductive potential of a marine ecosystem engineer at the edge of a newly expanded range. Global Change Biology 14:907–915

    Article  Google Scholar 

  27. Ling S, Johnson C, Frusher S, Ridgway K (2009a) Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proceedings of the National Academy of Sciences 106:22341–22345

    Article  Google Scholar 

  28. Ling S, Johnson C, Ridgway K, Hobday A, Haddon M (2009b) Climate-driven range extension of a sea urchin: inferring future trends by analysis of recent population dynamics. Global Change Biology 15:719–731

    Article  Google Scholar 

  29. Ling S, Scheibling R, Rassweiler A, Johnson C, Shears N, Connell S, Salomon A, Norderhaug K, Pérez-Matus A, Hernández J (2015) Global regime shift dynamics of catastrophic sea urchin overgrazing. Philosophical Transactions of the Royal Society B: Biological Sciences 370:20130269

    Article  Google Scholar 

  30. Ling SD, Mahon I, Marzloff M, Pizarro O, Johnson C, Williams S (2016) Stereo-imaging AUV detects trends in sea urchin abundance on deep overgrazed reefs. Limnology and Oceanography: Methods 14:293–304

    Google Scholar 

  31. Madin JS, Kuo C-Y, Martinelli JC, Mizerek T, Baird AH (2015) Very high coral cover at 36 S on the east coast of Australia. Coral Reefs 34:327

    Article  Google Scholar 

  32. McCook L, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral reefs 19:400–417

    Article  Google Scholar 

  33. Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98

    Article  CAS  PubMed  Google Scholar 

  34. Oliver EC, Lago V, Hobday AJ, Holbrook NJ, Ling SD, Mundy CN (2018) Marine heatwaves off eastern Tasmania: Trends, interannual variability, and predictability. Progress in Oceanography 161:116–130

    Article  Google Scholar 

  35. Pecl GT, Araújo MB, Bell JD, Blanchard J, Bonebrake TC, Chen I-C, Clark TD, Colwell RK, Danielsen F, Evengård B (2017) Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355:eaai9214

    Article  CAS  PubMed  Google Scholar 

  36. Pederson HG, Johnson CR (2006) Predation of the sea urchin Heliocidaris erythrogramma by rock lobsters (Jasus edwardsii) in no-take marine reserves. Journal of Experimental Marine Biology and Ecology 336:120–134

    Article  Google Scholar 

  37. Ridgway K (2007) Long‐term trend and decadal variability of the southward penetration of the East Australian Current. Geophys Res Lett 34:L13613. https://doi.org/10.1029/2007GL030393

  38. Strain E, Thomson RJ, Micheli F, Mancuso FP, Airoldi L (2014) Identifying the interacting roles of stressors in driving the global loss of canopy-forming to mat-forming algae in marine ecosystems. Global Change Biology 20:3300–3312

    Article  PubMed  Google Scholar 

  39. Stuart-Smith RD, Brown CJ, Ceccarelli DM, Edgar GJ (2018) Ecosystem restructuring along the Great Barrier Reef following mass coral bleaching. Nature 560:92–96

    Article  CAS  PubMed  Google Scholar 

  40. Tuckett C, de Bettignies T, Fromont J, Wernberg T (2017) Expansion of corals on temperate reefs: direct and indirect effects of marine heatwaves. Coral Reefs 36:947–956

    Article  Google Scholar 

  41. Tyberghein L, Verbruggen H, Pauly K, Troupin C, Mineur F, De Clerck O (2012) Bio-ORACLE: a global environmental dataset for marine species distribution modelling. Glob Ecol Biogeogr 21:272–281

    Article  Google Scholar 

  42. Valentine J, Edgar G (2010) Impacts of a population outbreak of the urchin Tripneustes gratilla amongst Lord Howe Island coral communities. Coral Reefs 29:399–410

    Article  Google Scholar 

  43. Valentine JP, Johnson CR (2004) Establishment of the introduced kelp Undaria pinnatifida following dieback of the native macroalga Phyllospora comosa in Tasmania, Australia. Marine and Freshwater Research 55:223–230

    Article  Google Scholar 

  44. Vergés A, Steinberg PD, Hay ME, Poore AG, Campbell AH, Ballesteros E, Heck KL, Booth DJ, Coleman MA, Feary DA (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 281:20140846

    Article  PubMed  Google Scholar 

  45. Vergés A, Doropoulos C, Malcolm HA, Skye M, Garcia-Pizá M, Marzinelli EM, Campbell AH, Ballesteros E, Hoey AS, Vila-Concejo A (2016) Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. Proc Nat Acad Sci 113:13791–13796

    Article  CAS  PubMed  Google Scholar 

  46. Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, De Bettignies T, Bennett S, Rousseaux CS (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nature Climate Change 3:78

    Article  Google Scholar 

  47. Wernberg T, Bennett S, Babcock RC, de Bettignies T, Cure K, Depczynski M, Dufois F, Fromont J, Fulton CJ, Hovey RK (2016) Climate-driven regime shift of a temperate marine ecosystem. Science 353:169–172

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Support was provided by ARC Linkage Project LP15010076 to GJE and NSB, and ARC Discovery Project DP170104668 to GJE and SDL. German Soler and Kate Fraser assisted in the field and Antonia Cooper assisted with management of the long-term data set. Australian Temperate Reef Collaboration field surveys were supported by Tasmanian Parks and Wildlife, Parks Victoria, New South Wales Department of Primary Industries, South Australian Department of Environment, Water and Natural Resources, and Western Australian Department of Biodiversity, Conservation and Attractions.

Author information

Affiliations

Authors

Contributions

All authors designed and performed field sampling; SDL wrote the draft manuscript; all authors edited the manuscript and acquired funding for the research.

Corresponding author

Correspondence to S. D. Ling.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Topic Editor Dr. Stuart A. Sandin

Appendices

Appendix 1

See Table 6.

Table 6 Summary of long-term temperate reef sampling sites by region, survey frequency, year range, and sampling area for each reef community component; i.e. algae/coral using in situ point intercept quadrats, and fishes plus invertebrates using belt transects

Appendix 2

See Tables 7, 8 and Fig. 7.

Table 7 Temperate Australia site-level analysis of hard coral cover and presence including “Depth” term in all models. (a) Cover of all hard corals (log + 0.001), (b) cover of P. versipora, (c) hard coral presence and (d) Plesiastrea presence
Table 8 Pearson correlation coefficients between predictor variables and coral presence/abundance for temperate Australian reef sites
Fig. 7
figure7figure7

Temperate Australia site-level patterns of hard coral presence and cover (ae) and P. versipora presence and cover (fj) versus sea surface temperature (SST), kelp canopy cover, herbivorous fish density, sea urchin density, and turf cover. Trend lines are binomial GLM fits of presence “1”/absence “0” data which is indicated on primary (left-hand side y axis); grey band gives the standard error for predictions about the fitted line; percentage cover data are overlaid as circles calibrated using right-hand y axis, with colouration by region (see legend adjacent to a). Direction of significant effects are indicated on each panel for presence, and cover data, respectively; ns non-significant effect, Significance codes are: “***”< 0.001; “**”< 0.01; “*”< 0.05

Appendix 3

See Table 9.

Table 9 Cover of P. versipora from 2004 to 2017 for kelp beds and Centrostephanus barrens at herbivory assay sites

Appendix 4

See Fig. 8.

Fig. 8
figure8

Example images of a kelp bed and Centrostephanus barrens habitats as sampled by 50 by 50 cm quadrats. a Kelp bed dominated by E. radiata and P. comosa, bCentrostephanus barrens dominated by high cover of encrusting coralline algae, with the urchin occurring at an effective density of 8 urchins m−2, cCentrostephanus barren dominated by high abundance of limpets, with the urchin occurring at a density of 4 m−2, dCentrostephanus barrens dominated by the coral P. versipora at an urchin density of 4 m−2

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ling, S.D., Barrett, N.S. & Edgar, G.J. Facilitation of Australia’s southernmost reef-building coral by sea urchin herbivory. Coral Reefs 37, 1053–1073 (2018). https://doi.org/10.1007/s00338-018-1728-4

Download citation

Keywords

  • Novel ecosystem
  • Tropicalization
  • Regime-shift
  • Temperate reefs
  • Climate change
  • Kelp beds